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Differences in relative abundance and size structure of the sea stars and Evasterias troschelii among habitat types in Puget Sound, Washington, USA

Article in Marine Biology · April 2012 DOI: 10.1007/s00227-012-2139-7

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ORIGINAL PAPER

Differences in relative abundance and size structure of the sea stars Pisaster ochraceus and Evasterias troschelii among habitat types in Puget Sound, Washington, USA

Tanya L. Rogers • Joel K. Elliott

Received: 11 July 2012 / Accepted: 23 November 2012 / Published online: 23 December 2012 Ó Springer-Verlag Berlin Heidelberg 2012

Abstract We surveyed patterns in the relative abundance consumer related to a shared risk at early and size structure of the sea stars Pisaster ochraceus and life stages and demonstrate how the relative importance of Evasterias troschelii in five habitat types of varying top-down and bottom-up processes may differ with structural complexity and prey availability (sand/cobble, ontogeny. boulder, and rocky intertidal; pilings; and floating docks) in Puget Sound and the San Juan Islands, Washington. For both species, small sea stars were most abundant in the Introduction most structurally complex habitat type (boulder), where they occurred almost exclusively under boulders during The relative importance of bottom-up and top-down pro- low tide. Larger individuals became more abundant as cesses within communities is known to be dependent on structural complexity decreased, occurring more frequently environmental context (Hunter and Price 1992, Menge in open habitat types (rocky shores, pilings, and docks) 2000). The two are often coupled in the sense that changes known to have greater abundances of prey resources. Gull in environmental factors such as nutrient availability or foraging observations and experiments demonstrated that flow regime may alter not only productivity, but also pre- exposed small sea stars of both species were highly vul- dation intensity and subsequent top-down effects (Menge nerable to predation, suggesting that small sea stars require et al. 1997, 1999; Leonard et al. 1998; Menge 2000; structural complexity (crevice microhabitat) as a predation Nielsen 2001). Habitat structure is known to have a par- refuge. Large sea stars, once attaining a size refuge from ticularly strong influence on predation intensity, which is predation, appear to migrate to more exposed habitat types generally found to be lower in areas of high structural with more abundant food resources. These results suggest complexity due to the presence of prey refugia (Crowder parallel ontogenetic habitat shifts in two co-occurring and Cooper 1982; Power 1992; Dahlgren and Eggleston 2000). As a result, habitat structure and refuge quality may affect the recruitment and survival rates of species or life Communicated by M. Byrne. stages that are vulnerable to predation (Keough and Downes 1982; Eggleston and Armstrong 1995; Jordan Electronic supplementary material The online version of this article (doi:10.1007/s00227-012-2139-7) contains supplementary et al. 1996). material, which is available to authorized users. Consumer species often occupy different habitats throughout their life history, and these habitats often vary & T. L. Rogers Á J. K. Elliott ( ) in both structural complexity and food availability (Werner Department of Biology, University of Puget Sound, Tacoma, WA 98416, USA and Gilliam 1984; Dahlgren and Eggleston 2000; Snover e-mail: [email protected] 2008). Size-dependent predation risk and ontogenetic changes in prey preference are thought to be the main Present Address: contributors to these habitat shifts, as species may face a T. L. Rogers Florida State University Coastal and Marine Lab, trade-off between maximizing growth and minimizing 3618 Hwy 98, St. Teresa, FL 32358, USA predation risk as they advance in their life cycle (Werner 123 854 Mar Biol (2013) 160:853–865 and Gilliam 1984; Schmitt and Holbrook 1985; Snover Rogers and Elliott, personal observation), yet despite 2008). Among benthic invertebrates, predation in particular Evasterias’s high abundance in Puget Sound, very little is is considered to be the most important cause of juvenile known about its ecology besides its general feeding habits mortality, resulting in greater abundances of juveniles in (Christensen 1957; Mauzey et al. 1968; Young 1984). The more structurally complex habitats and microhabitats that relationship between Pisaster and Evasterias, two over- provide shelter from predators (Heck and Wetstone 1977; lapping and potentially interacting predator species, has not Keough and Downes 1982; Gosselin and Quian 1997). been investigated, although the relationship between them Interspecific interactions may also change with ontogeny, is predicted to be highly competitive (Menge 1972; Menge with implications for the larger community (Werner and and Menge 1974). Gilliam 1984). Understanding the relative importance of Several studies have shown that sea star species undergo top-down and bottom-up processes throughout the life an ontogenetic shift in habitat use, with early life stages history of a species is therefore important in illuminating more abundant in different habitats than larger juveniles both the causes and consequences of these ontogenetic and adults (Himmelman and Dutil 1991; Verling et al. shifts in habitat use. 2003; Scheibling and Metaxas 2008, 2010; Bos et al. 2010; We examined the distributions, size structure, and rel- Manzur et al. 2010). The objective of this study was to ative abundances of two intertidal sea star species across examine patterns in the relative abundance and size dis- habitats of varying structural complexity (predator sus- tribution of Pisaster and Evasterias in five different habitat ceptibility) and resource availability to investigate the types of varying structural complexity and prey availability relative importance of top-down and bottom-up processes (sand/cobble intertidal, boulder intertidal, rocky intertidal, on the different life history stages of these consumers. The pilings, and floating docks) in the Puget Sound and San sea star Pisaster ochraceus (hereafter, Pisaster) is a key- Juan Island regions. This included an examination of the stone predator in the northeast Pacific that is known to microhabitat use of sea stars in structurally complex hab- drive patterns in species diversity and intertidal zonation itats. To help explain the observed distribution patterns, we (Paine 1966, 1974; Menge et al. 1994, 2004; Robles et al. also investigated the risk of Pisaster and Evasterias of 1995, 2009). Although the community impacts of Pisaster varying sizes to predation by gulls through gull foraging are relatively well understood, most studies have focused observations, prey preference experiments, and measures exclusively on the activity of larger juvenile and adult sea of sea star attachment strength. Preliminary observations in stars, which are common and conspicuous in rocky inter- Puget Sound suggested that gulls (Laurus sp.) preyed tidal communities. Additionally, the habitat types in which heavily on small individuals of both Pisaster and Evaste- Pisaster have been studied have been largely limited to rias (Elliott and Rogers, personal observation). Given that rocky intertidal habitats on the outer Pacific coast (e.g., gull predation has been shown to have major effects on Feder 1959; Paine 1966, 1974; Menge et al. 1994; Robles populations of other intertidal invertebrates (e.g., Wootton et al. 1995, 2009) and in the San Juan Islands of Wash- 1992, 1997; Ellis et al. 2005, 2007) and that gulls have ington state (e.g., Mauzey 1966; Menge and Menge 1974; been observed feeding on intertidal sea stars in a number of Harley et al. 2006). However, Pisaster also occur in a different geographic locations (Sibly and McCleery 1983; variety of other habitat types, including cobble/boulder Irons et al. 1986; Wootton 1997; Verling et al. 2003; beaches and on man-made structures (e.g., pilings and Snellen et al. 2007; Suraci and Dill 2011), we chose to floating docks) at more sheltered locations. In Puget Sound, examine gull predation on Pisaster and Evasterias, as well Washington, rocky habitat typical of the outer coast is rare, as differences in the vulnerability of both species to gull and cobble/boulder beaches and man-made structures such predation, as a potential top-down mechanism for differ- as breakwaters, docks and pilings make up a substantial ences in sea star size distributions among habitat types and proportion of the hard substratum available as habitat for differences in sea star microhabitat use. Pisaster (Bailey et al. 1998). The way in which Pisaster uses these alternative habitat types, which vary in structural complexity and food resources, is largely undocumented Materials and methods (except see Feder 1959, 1970; Pearse et al. 2009). Evasterias troschelii (hereafter, Evasterias) is another Habitat types predatory sea star species that co-occurs with Pisaster in Puget Sound, the San Juan Islands, and along the Strait of The habitat types surveyed for sea stars were sand/cobble Juan de Fuca, but is not common on the exposed outer intertidal, boulder intertidal, rocky intertidal, pilings, and coast (Mauzey et al. 1968). Evasterias utilizes intertidal floating docks. Sand/cobble habitats were defined as sandy and subtidal habitat types and prey resources very similar beaches interspersed with mostly pebbles and cobbles to those of Pisaster (Lambert 2000; Mauzey et al. 1968; (\20 cm in diameter). Boulder habitats were shorelines 123 Mar Biol (2013) 160:853–865 855 consisting primarily of rocks 20–40 cm in diameter. Rock habitats surveyed were located in Puget Sound, and most habitats were shorelines composed of either solid bedrock rock habitats surveyed were located in the San Juan or rocks [40 cm in diameter (natural rock or concrete Islands. We surveyed many of the same areas as Menge riprap). Piling habitat included nearshore wooden or con- (1972) and Menge and Menge (1974), who provide crete pilings, either supporting a structure or free-standing. detailed descriptions of the sites. Dock habitats were floating docks typically made of con- For all Pisaster and Evasterias located within each crete that had been in place for more than a decade and had survey area, we recorded arm length (radius) measured established fouling communities. Although not intertidal, from the center of the oral disk to the tip of the straightest floating docks are very common in Puget Sound and can arm, excluding arms that were clearly damaged or regen- host sizable communities of sea stars and their invertebrate erating. For sea stars in unreachable locations, we either prey (Elliott et al. 2008), so we include them in our study. estimated arm length or recorded only the presence of the Boulder habitats were the most structurally complex of individual for use in measurements of relative abundance, the five habitats, offering the most crevice space that could but not size distribution. For sand/cobble, boulder, rock, be inhabited by sea stars. Sand/cobble and rock habitats and piling habitats, we surveyed all sea stars in the inter- were of intermediate complexity, offering some crevice tidal zone to maximize the number of individuals that space. Piling and dock habitats were the least complex, could be measured for size distribution analyses, as done offering little or no crevice space. We surveyed only the by Feder (1970), Pearse et al. (2009), and Manzur et al. sides of the docks, although crevices between dock sections (2010). We surveyed all sea stars found on the vertical and the bottoms of the docks may have provided shelter sides of floating docks. When surveying boulder habitats, from predators such as gulls. all boulders that were movable (approximately \40 cm in diameter) were overturned, examined for sea stars, and Sea star field surveys replaced. Sea stars were rarely found under rocks smaller than 20 cm in diameter, so these small rocks were typically We surveyed the five habitats types for the sea stars not overturned, allowing time to survey a larger area. Pisaster and Evasterias at 39 different locations in the San While surveying boulder sites in Puget Sound, we recorded Juan Island and Puget Sound regions of Washington state the microhabitat use of each sea star in addition to size, (Fig. 1; Table 1). We conducted the majority of surveys noting whether individuals were found in the open (plainly during the summer of 2009 (May–August) and included visible) or concealed under a boulder. We also measured additional survey data from the summers of 2005, 2008, the mass of a subset of sea stars in the field using a spring and 2010. All surveys were conducted during daytime scale in order to quantify the relationship between mass negative low tides with the exception of floating docks, and arm length for each species. which were surveyed at any time during daylight hours. For each habitat type, we combined data from all sites to At many sites, multiple habitat types were surveyed. Due to create size frequency distributions. We compared the differences in the coastal substratum and in the prevalence median arm length of Pisaster and Evasterias among of man-made structures between regions (Bailey et al. habitat types using Mann–Whitney U tests with a Bonfer- 1998), all sand/cobble habitats and most dock and piling roni adjustment for multiple comparisons (a = 0.005). For

Fig. 1 Map of study sites where sea star surveys were conducted in a Puget Sound and b the San Juan Islands, Washington, USA. Numbers correspond to site details are given in Table 1

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Table 1 List of study sites shown in Fig. 1 where sea star surveys were conducted Regions Site # Sites Latitude Longitude Habitat

Puget Sound 1 Titlow* 47.253840° -122.552615° Boulder Puget Sound 1 Titlow north* 47.254998° -122.551861° Sand/cobble Puget Sound 2 Fox Island* 47.275350° -122.650202° Rock; piling Puget Sound 2 Fox Island* 47.273782° -122.653238° Sand/cobble Puget Sound 2 Tanglewood 47.264519° -122.644041° Dock Puget Sound 3 Kopachuck* 47.310763° -122.688583° Sand/cobble Puget Sound 4 Joemma Beach 47.224747° -122.810538° Sand/cobble Puget Sound 5 Ruston Sundial 47.275842° -122.462055° Boulder Puget Sound 5 Johnny’s* 47.276882° -122.464675° Dock Puget Sound 5 Johnny’s 47.276501° -122.465391° Piling Puget Sound 6 Ruston Way 47.281885° -122.478948° Boulder Puget Sound 6 Ruston Way 47.282125° -122.479274° Piling Puget Sound 6 Ruston Way 47.281422° -122.478087° Rock Puget Sound 6 Les Davis pier 47.283562° -122.481266° Piling Puget Sound 6 ASARCO* 47.294793° -122.497688° Boulder Puget Sound 7 Pt. Defiance marina* 47.305655° -122.512732° Piling Puget Sound 7 Pt. Defiance east 47.306660° -122.515945° Boulder Puget Sound 7 Pt. Defiance east 47.306869° -122.516297° Piling Puget Sound 7 Pt. Defiance east* 47.306660° -122.515945° Rock Puget Sound 7 Pt. Defiance west 47.307152° -122.517938° Boulder Puget Sound 7 Pt. Defiance west 47.307289° -122.517813° Piling Puget Sound 7 Pt. Defiance west* 47.307292° -122.518588° Sand/cobble Puget Sound 8 Gig Harbor 1 47.330517° -122.578337° Dock Puget Sound 8 Gig Harbor 2 47.332089° -122.580432° Dock Puget Sound 9 Dockton 1* 47.372427° -122.453712° Dock Puget Sound 9 Dockton 1 47.372427° -122.453712° Piling Puget Sound 9 Dockton 2 47.371795° -122.453914° Piling Puget Sound 10 Maury Island* 47.362893° -122.439812° Piling Puget Sound 11 Des Moines 47.401653° -122.329809° Dock Puget Sound 12 Manchester 47.578259° -122.545577° Boulder Puget Sound 12 Manchester* 47.577336° -122.543945° Rock Puget Sound 12 Manchester 47.553817° -122.541952° Sand/cobble Puget Sound 13 Silverdale* 47.642171° -122.694284° Dock Puget Sound 13 Silverdale 47.642724° -122.694687° Piling San Juan Is. 1 Davis Reef 48.457118° -122.939595° Rock San Juan Is. 2 Cattle Point 48.450787° -122.961749° Boulder San Juan Is. 2 Cattle Point 48.450787° -122.961749° Rock San Juan Is. 3 Eagle Cove 48.460289° -123.033297° Rock San Juan Is. 4 Deadman Bay 48.512985° -123.147132° Rock San Juan Is. 5 Snug Harbor 48.571844° -123.169627° Boulder San Juan Is. 5 Snug Harbor 48.571844° -123.169627° Rock San Juan Is. 6 Turn Rock 48.535345° -122.964733° Rock San Juan Is. 7 Pt. Caution 48.561845° -123.017814° Boulder San Juan Is. 7 Pt. Caution 48.562142° -123.017295° Rock San Juan Is. 8 Reuben Tarte 48.613055° -123.097457° Boulder San Juan Is. 8 Reuben Tarte 48.613055° -123.097457° Rock San Juan Is. 9 Lonesome Cove FP 48.621732° -123.117102° Boulder San Juan Is. 9 Lonesome Cove FP 48.622021° -123.117101° Rock

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Table 1 continued Regions Site # Sites Latitude Longitude Habitat

San Juan Is. 9 Lonesome Cove RA 48.621031° -123.112466° Boulder San Juan Is. 9 Lonesome Cove RA 48.621430° -123.111788° Rock San Juan Is. 10 Yellow Island 48.593160° -123.030191° Boulder San Juan Is. 10 Yellow Island 48.593160° -123.030191° Rock San Juan Is. 11 Jones Island 48.618095° -123.048611° Boulder San Juan Is. 11 Jones Island 48.618674° -123.048184° Rock San Juan Is. 12 Deer Harbor 48.621144° -123.004347° Dock San Juan Is. 13 West Sound 48.629073° -122.959961° Dock San Juan Is. 13 West Sound 48.629388° -122.957061° Piling San Juan Is. 14 Gull Reef 48.654583° -123.146862° Rock San Juan Is. 15 Ripple Island 48.657572° -123.130221° Boulder San Juan Is. 15 Ripple Island 48.657572° -123.130221° Rock San Juan Is. 16 Sucia Island 48.764138° -122.914258° Boulder San Juan Is. 16 Sucia Island 48.752437° -122.904723° Dock San Juan Is. 16 Sucia Island 48.764763° -122.919469° Rock Sites with asterisks were also surveyed for sea star prey abundance (Fig. 5) boulder habitats in Puget Sound, we compared sea star to the difficulty of obtaining accurate counts from photo- sizes between microhabitat types using t tests. graphs for this habitat. We calculated the density per site of Pisaster and Evasterias as the number of sea stars per area surveyed. For Risk of sea stars to gull predation sand/cobble, boulder, and rock habitats, the survey area was calculated from the length of shoreline surveyed and We observed the natural foraging behavior of gulls (Laurus the approximate width of shoreline over which sea stars sp.) and their predation on sea stars in four habitat types occurred (this distance varied depending on slope of shore). (boulder, rock, piling, and dock) using a spotting scope Lengths of shorelines were measured using either mea- (Swarovski ATM-65) or camera with a telephoto lens suring tapes in the field or satellite images in Google Earth (Nikon D300 s with 200-mm lens). We recorded the spe- Pro using known GPS coordinates or identifiable site cies of all sea stars consumed or attacked and estimated the markers in the satellite images. For pilings, the survey area size of each sea star as either small (\6 cm in arm length), was calculated based on the number of pilings surveyed, medium (6–14 cm), or large ([14 cm). Pisaster \7.4 cm the piling circumference, and the vertical range over which in arm length are considered immature (Menge and Menge sea stars occurred (typically 4 m). For docks, the survey 1974), so our small size category encompassed exclusively area was the total area of dock sides surveyed. We com- immature individuals for this species. In intertidal habitats, pared the densities of sea stars among habitat types using gull foraging was observed during low tide. one-way ANOVA and t tests. To determine the susceptibility of exposed sea stars of different sizes to predation by gulls, we conducted prey Prey availability selection experiments in which gulls were simultaneously offered a small (4–6 cm), medium (9–11 cm), and large We ranked the five habitats for food availability using ([14 cm) sea star. Ten trials were conducted with a size descriptions from the literature, which were in many cases range of Pisaster, and 10 trials were conducted with a size of the same study sites in the San Juan Islands (Mauzey range of Evasterias. During low tide in an area where gulls 1966; Menge and Menge 1974) and in Puget Sound (Elliott were foraging, the three different sizes of sea stars were et al. 2008), and using quantitative prey quadrat data from placed in the open on sand or algae (so the sea stars could sites in Puget Sound. We identified and counted the number not attach) near the low tide line in a triangular arrange- of sea star prey present in 30 25 9 25 cm photograph ment with approximately 40 cm between the center of each quadrats per habitat type, 10 each from 3 representative sea star. We recorded which sea stars were attacked and sites in Puget Sound (Fig. 1; Table 1). Mussels on docks consumed by gulls. The trials were conducted in boulder were counted through destructive sampling of quadrats due and sand/cobble habitats (Pt. Defiance and Ruston Way), as

123 858 Mar Biol (2013) 160:853–865 these habitats were where gulls most frequently foraged stars found in boulder habitats in the Puget Sound region, and where it was most convenient to set up and observe the the majority of sea stars were found underneath rocks, and predation experiments. these sea stars were significantly smaller than those found

To test for differences in the attachment strength of out in the open (t test, Pisaster: t178 =-12.00, P \ 0.001; Pisaster and Evasterias, we measured the force required to Evasterias: t292 =-13.91, P \ 0.001). No sea stars pull sea stars from natural substrata. The sea stars varied in \8 cm arm length were found in the open in boulder size from 1.0 to 10 cm in arm length (n = 46 Pisaster,43 habitats, and small sea stars were rarely observed in the Evasterias). At three boulder sites (Titlow, ASARCO, and open in any of the other habitat types. Sea stars of both Pt. Defiance east), we overturned rocks at low tide and species tended to be larger in the San Juan Islands than in located sea stars with all five arms firmly attached to the Puget Sound within a given habitat type. rock surface. A clamp or cable tie was attached to one arm of each sea star (adjacent to the central disk), which was Sea star relative abundance then connected by a cable to a spring balance (10 kg capacity). Sea stars were gently prodded before attaching Sea star densities varied among habitat types, with the the clamp or cable tie to ensure that they were firmly highest densities of both Pisaster and Evasterias occurring attached to the substratum. The sea star was then pulled off on pilings (Pisaster: ANOVA, F(4,51) = 14.37, P \ 0.001; the boulder perpendicular to the substratum at roughly Evasterias: ANOVA, F(4,51) = 8.92, P \ 0.001; Fig. 4). constant acceleration, and the maximum force displayed on With the exception of dock habitats, the density of Pisaster the spring balance was recorded. The mass of the clamp appeared to increase with increasing prey abundance, and sea star was subtracted from the force required to although the differences in densities between sand/cobble, remove the sea star. We examined the effect of sea star size boulder, and rock habitats were not statistically significant. (arm length) and species on attachment strength using The second highest density of Evasterias occurred in ANCOVA. boulder habitats (the most structurally complex environ- ment), with low densities occurring in the remaining hab- itat types. Patterns in the biomass per unit area of both Results species (derived from regressions in Online Resource 1) were consistent with these trends. Sea star size structure The density of Pisaster was significantly higher than that

of Evasterias in rock (t test, t34 =-3.31, P = 0.002), For both sea star species, size frequency distributions piling (t20 =-2.54, P = 0.020), and dock (t12 =-2.49, varied substantially among habitats (Fig. 2). Small indi- P = 0.029) habitats. Densities of Pisaster and Evasterias viduals (\6 cm in arm length) were only abundant in the did not differ in boulder habitats (t26 = 0.81, P = 0.42), most structurally complex habitat (boulder) and were rare and the density of Evasterias was significantly higher than in other habitat types (except for Evasterias in rock habi- that of Pisaster in sand/cobble habitats (t10 = 2.612, tat). Pilings and docks, the most open habitats, had low P = 0.026). On average, over 90 % of the sea stars found in frequencies of small sea stars for both species, and the sand/cobble habitat were Evasterias. Due to unequal sam- greatest frequencies of larger individuals. Trends in median pling of habitat types between regions, we could not accu- sea star size are consistent with this pattern: For both rately test for differences in sea star density between Puget species, the median size of sea stars was smallest in Sound and the San Juan Islands, except in boulder habitats, boulder habitats, followed by rock, piling, and dock habi- where we found no significant difference in the densities of tats (Mann–Whitney U test, Bonferroni corrected, either species between regions (t tests, P [ 0.05). P \ 0.005), although Pisaster did not differ in median size between piling and dock habitats. In sand/cobble habitats, Prey availability Evasterias were comparable in size to Evasterias in rock habitats. Pisaster in sand/cobble habitat were rare and (Balanus spp.) and mussels (Mytilus spp.) were the typically large in size. Within a given habitat type, Pisaster most common prey found in the five habitat types (Fig. 5). were similar in arm length to Evasterias, but Pisaster were Other prey types present included large barnacles (Semi- much larger in mass (Online Resource 1). A typical large balanus cariosus), which were only common in rock and Pisaster of 15 cm in arm length (565 g) was approximately piling habitats, and (Lottia spp.) which were most 1.8 times the mass of an Evasterias of the same arm length abundant in the intertidal habitats. Sand/cobble habitats had (315 g). the lowest availability of prey, as there was a limited amount Sea stars of different sizes also exhibited differences in of hard substratum available for the attachment of sessile microhabitat use in boulder habitats (Fig. 3). Of the sea invertebrates. Boulder habitats had the next lowest prey 123 Mar Biol (2013) 160:853–865 859

30 Evasterias30 Pisaster Resource Structural 25 25 sand/cobble sand/cobble availability complexity (146) (10) 20 20 lowest medium x = 13.57 x = 14.70 15 15

10 10

5 5

0 0 0 4 8 12 16 20 24 28 32 36 0 4 8 12 16 20 24 28 32 36 30 30

25 25 boulder boulder 20 (351) 20 (241) high x = 7.68 x = 9.23 15 15

10 10

5 5

0 0 0 4 8 12 16 20 24 28 32 36 0 4 8 12 16 20 24 28 32 36 30 30

25 25 rock rock 20 (86) 20 (692) medium x = 12.71 x = 12.83 15 15 percent percent 10 10

5 5

0 0 0 4 8 12 16 20 24 28 32 36 0 4 8 12 16 20 24 28 32 36 30 30

25 piling 25 piling (109) (219) 20 20 low x = 15.77 x = 15.77 15 15

10 10

5 5

0 0 0 4 8 12 16 20 24 28 32 36 0 4 8 12 16 20 24 28 32 36 30 30

25 dock 25 dock (37) (242) 20 20 x = 19.25 x = 15.93 highest low 15 15

10 10

5 5

0 0 0 4 8 12 16 20 24 28 32 36 0 4 8 12 16 20 24 28 32 36 arm length (cm) arm length (cm)

Fig. 2 Size frequency distributions of Pisaster and Evasterias in five habitat types. Numbers in parentheses indicate sample sizes. Black triangles indicate location of means

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30 12000 Evasterias c Balanus 10000 25 (259) Mytilus 8000 b 20 (35) 6000 b C 15 4000

10 2000 a B Individuals per square meter AA A 0 9.9 a 5 0 sand/cobble boulder rock piling dock Habitat 0 45 Fig. 5 Densities of mussels (Mytilus spp.) and barnacles (Balanus

percent (147) 40 spp.) found in five habitat types (n = 30 25 9 25 cm quadrats per Pisaster habitat, taken from 3 different sites as indicated in Table 1). Analyses 35 were performed for each prey type independently: shared letters on 30 (33) in open bars indicate no significant difference in density between habitat types (ANOVA, P [ 0.05) 25 under cobble

20 intertidal), but mussels were rare in this habitat and com- 15 pletely absent from boulder and sand/cobble habitats 10 (Mauzey 1966; Menge and Menge 1974). Prey resources 5 were greatest on pilings and floating docks, which had the 0 highest abundances of mussels (the preferred prey item of 0 4 8 12 16 20 24 28 32 36 Pisaster; Mauzey et al. 1968). Although mussels were arm length (cm) numerically more abundant on pilings, the mussels on docks were substantially larger, so overall mussel biomass was Fig. 3 Microhabitat use of Pisaster and Evasterias in Puget Sound greatest on docks (Elliott et al. 2008). We therefore ranked Numbers in parentheses boulder habitats. indicate sample sizes for each docks highest in terms of prey availability. size frequency distribution. Black triangles indicate location of means

Risk of sea stars to gull predation B 30 Evasterias * 25 Pisaster Juvenile and adult Glaucous-wing Gulls (Larus glauces- cens, and potentially some hybrids with Western Gulls, 20 Larus occidentalis) were observed feeding on sea stars in 15 c all habitat types. Gulls were most frequently observed foraging in boulder habitats during low tide, where they 10 * A

Sea star density b were seen searching for and pulling reachable sea stars out A 5

(# individuals / 100 m² ) * * A from under boulders. We observed 116 attacks by gulls on ab a ab A (14) (18) (11) (7) 0 (6) sea stars at 12 locations in 24 h of observation time sand/cobble boulder rock piling dock (Table 2). The majority of observation time (84 %) was Resource lowest highest availability spent in boulder habitats, as that was where gulls were most Structural often observed foraging during low tide. Most attacks complexity medium high medium low low Habitat (78 %) were therefore observed in boulder habitats. Within boulder habitats, small and medium-sized sea Fig. 4 Density of Pisaster and Evasterias (mean per site ± SE) in five stars were preyed upon most frequently (56 and 42 % of habitat types. Numbers in parentheses indicate sample sizes. Analyses observations, respectively), and Evasterias were preyed were performed for each species independently: shared letters on bars indicate no significant difference in density between habitat types upon more frequently than Pisaster (88 % of observations). (ANOVA, P [ 0.05). *Significant difference between density of Boulder habitats had approximately equal densities of Pisaster and Evasterias within a habitat type (t test, P [ 0.05) Pisaster and Evasterias (Fig. 4); however, of the sea stars in boulder habitats within the size range consumable by availability, followed by rock habitats. Rock habitats had the gulls, approximately 70 % were Evasterias. Small and highest densities of barnacles (Balanus glandula are known medium sea stars were swallowed whole, the smallest in a to make up 75 % of the total prey in the San Juan Island rocky few seconds, the medium-sized individuals taking up to an 123 Mar Biol (2013) 160:853–865 861

Table 2 Observations of gull Species Size Arm Habitat Percent predation on sea stars in length (cm) different habitat types Boulder Rock Piling Dock

Evasterias Small \6 43 0 1 0 37.9 Medium 6–14 35 5 1 4 38.8 Large [14 1 0 0 8 7.8 Pisaster Small \6 7 1 1 0 7.8 Medium 6–14 3 1 0 3 6.0 Large [14 1 0 0 1 1.7 Total sea stars attacked 90 7 3 16 Percent Evasterias 87.8 71.4 66.7 75.0 84.5 Percent Pisaster 12.2 28.6 33.3 25.0 15.5

hour, particularly for Pisaster. When attacking large-sized 100 Evasterias sea stars, gulls would turn them over and peck at tube feet 80 Pisaster in the ambulacral grooves and in two instances pulled arms off of large Evasterias by shaking them. 60 We observed gulls pulling small Pisaster and all sizes of Evasterias off the substratum, but they had difficulty 40 pulling off all but the most loosely attached medium 20 Pisaster. Gulls were never observed pulling off firmly consumed Percentage 0 0 0 attached large Pisaster. It is likely that the large and 0 medium Pisaster we observed being attacked by gulls had Small Medium Large Sea star size been on a loose substratum (e.g., sand/gravel, mussel bed on a dock), which enabled them to be easily removed and Fig. 6 Frequencies at which sea stars of varying sizes were overturned by gulls. consumed by gulls when gulls were simultaneously presented with In the prey selection experiments, gulls attacked and one small (4–6 cm), medium (9–11 cm), and large ([14 cm) sea star (n = 10 trials for Pisaster and 10 trials for Evasterias). Gulls pecked consumed the small sea stars first in all 10 trials for at medium Pisaster in 50 % of trials, but did not consume them Pisaster and Evasterias (Fig. 6). Gulls then attacked the medium-sized Evasterias in all trials and consumed them 5 in 7 of 10 trials. Medium-sized Pisaster were pecked at in 5 4.5 Evasterias Pisaster of 10 trials, but gulls never consumed these sea stars. Gulls 4 typically ignored the large sea stars of both species and did 3.5 not attempt to feed on them. The arm length below which 3 both sea star species were vulnerable to lethal predation 2.5 (swallowing) corresponded to a body mass of approxi- 2 mately 200 g (9 cm arm length for Pisaster and 12 cm arm length for Evasterias). 1.5 For both species, attachment strength increased signifi- 1

ln attachment strength (N x 10^3) ln attachment 0.5 cantly with sea star size (ANCOVA, F(1,85) = 55.26, P \ 0.001; Fig. 7). The rate of increase in attachment 0 strength with arm length was greater for Pisaster than for 0 0.5 1 1.5 2 2.5 Evasterias (unequal slopes; ANCOVA, mass * species, ln arm length (cm) F(1,85) = 5.39, P = 0.023). When attachment strength and Fig. 7 Attachment strength of Pisaster (n = 26) and Evasterias sea star size data were natural log transformed, slopes did (n = 37) of varying sizes, and double logarithmic linear regressions not significantly differ between species (ANCOVA, for each species. Pisaster R2 = 0.673; Evasterias R2 = 0.481

F(1,85) = 1.13, P = 0.292), and there was a significant difference in attachment strength between species Discussion

(ANCOVA, F(1,85) = 8.52, P = 0.005). Pisaster had approximately 1.3 times greater attachment strength than Our field surveys demonstrated differences in the size Evasterias for given arm length. structure and relative abundance of Pisaster and Evasterias 123 862 Mar Biol (2013) 160:853–865 among habitat types, which appear related to variation in Prey preference in sea stars, including Pisaster,is structural complexity and food availability. For both species, known to vary as individuals increase in size, with larger the abundance of small sea stars increased with increasing sea stars tending to consume larger prey (Paine 1976; habitat complexity, while larger individuals became more Menge and Menge 1974; Sloan 1980; Tokeshi et al. 1989; abundant as structural complexity decreased. Small sea stars Manzur et al. 2010). Pisaster are also known to be quite were most abundant in boulder habitats, where they occurred mobile in the intertidal (Feder 1956; Feder and Christensen almost exclusively under boulders, whereas larger sea stars 1966) and to increase in density in areas with greater food occupied the more open habitats (rocky shores, pilings, and abundance (specifically areas of high mussel recruitment; docks) with greater abundances of prey resources (mussels Robles et al. 1995, 2009), so it is reasonable that they and barnacles). Gull feeding observations and experiments might move between habitats types in search of greater demonstrated that small sea stars, particularly those\6cm prey resources once they ‘‘outgrow’’ their existing resour- arm length, were highly vulnerable to predation, and large ces and no longer require shelter. Pisaster are also thought sea stars, although subject to ambulacral pecking if detached to require an abundance of large mussels to attain large from the substratum, possessed a size refuge. These results sizes, and to not grow as large in sheltered intertidal hab- suggest that small sea stars require crevice microhabitat as a itats, where barnacles and limpets constitute their main predation refuge. Interestingly, Pisaster \7.4 cm in arm prey (Mauzey 1966; Feder 1970). length are considered to be immature (Menge and Menge We suspect that the low densities of sea stars found in 1974), which suggests there may be strong selection for dock habitats are the result of the limited accessibility of small Pisaster to put energy into growth until they reach a floating docks to sea stars. The only way for sea stars to get size less vulnerable to predation. Large sea stars, once onto most floating docks is to crawl onto them from the attaining this size refuge, appear to move to habitat types support pilings (a physically difficult task given the large with more abundant food resources, which is also supported gap between most support pilings and their associated by the apparent increase in Pisaster density with increasing docks), or to recruit onto them directly as larvae. Smaller, prey availability (the exception of docks is discussed below). newly recruited sea stars on docks would be highly vul- In summary, the distribution of small sea stars appears to be nerable to predation by gulls (and potentially subtidal driven primarily by top-down pressures, whereas bottom-up predators), and they were rarely observed on the sides of factors appear more important in determining the distribu- docks, so growth of recruits to adults may be rare. Sea stars tion of adult sea stars. that do manage to get onto a dock would have access to an In studies of other sea star species, juveniles were found to abundance of food resources, few competitors, and the occur in habitats with high structural complexity (e.g., ability to forage continuously without the interruption of boulders, mangroves, and seagrass), and larger individuals low tides. This may allow them to attain the large sizes that were found in more open habitats with larger and more we observed on docks. profitable food resources (Himmelman and Dutil 1991; Gulls have been found to consume sea stars in the Verling et al. 2003; Scheibling and Metaxas 2008, 2010; Bos Northeast Pacific, but in the majority of these studies, sea et al. 2010; Manzur et al. 2010). Susceptibility of small stars comprised only a very small proportion of gull diets individuals to predation pressures and ontogenetic changes (Vermeer 1982; Irons et al. 1986; Wootton 1997; Snellen in prey preference are explanations commonly given for et al. 2007), and these predators had not been considered to these patterns (Snover 2008), and our study similarly sug- have a significant effect on sea star populations (Lambert gests an ontogenetic habitat shift occurring for Pisaster and 2000). Our study, in contrast, suggests high rates of pre- Evasterias.ForPisaster, our results are consistent with the dation by gulls on sea stars, which appear to have a strong observations of Feder (1970) in Monterey Bay, who only influence on sea star sizes and habitat use. Pearse et al. observed small Pisaster under boulders or deep in crevices. (2009) observed Western Gulls pecking at the ambulacral Whether sea stars selectively recruit to boulder habitats and and oral areas of overturned large Pisaster, but to our crevices or whether they have higher post-settlement sur- knowledge, only one published study (Suraci and Dill vival in these habitat types is unknown. Our observations in 2011) quantitatively documents moderate to high rates of Puget Sound suggest the latter, as we have observed high predation by gulls on Pisaster. In the context of optimal recruitment of sea stars (primarily Evasterias) to all habitat foraging, Suraci and Dill (2011) describe predation by types in the fall, but by the spring, small sea stars were only Glaucous-winged Gulls on small Pisaster in the Strait of found in crevices or under boulders (Elliott and Rogers, Georgia, British Columbia. They found the size range of personal observation). In one of the few studies of Pisaster Pisaster susceptible to gull predation to be 0.8–8.6 cm arm recruitment, Sewell and Watson (1993) likewise found that length, which is consistent with our findings. High rates of newly recruited Pisaster (\1 cm) experienced[97 % mor- predation by gulls on sea stars therefore appear to be tality, and very few survived to be 1 year old. localized to certain geographic regions, such as the 123 Mar Biol (2013) 160:853–865 863 sheltered areas of the Puget Sound/Georgia Basin. Pisaster could potentially account for the greater abundances of are abundant on the outer Washington coast and in other Pisaster than Evasterias in rock, piling, and dock habitats, locations such as Monterey Bay, but gull predation is rarely which are also the habitats with the greatest prey resources. observed there, likely because small Pisaster are relatively In summary, our study highlights that the relative rare. Pisaster may also be more strongly attached on the importance of top-down and bottom-up processes may differ exposed rocky coast than in less exposed areas. The main across life stages, and this may be a major driver of patterns intertidal prey of gulls on the outer coast of Washington are in habitat use. Unlike most studies on ontogenetic habitat gooseneck barnacles (Wootton 1997), but in Puget Sound, shifts in sea stars, we describe size and habitat patterns in where gooseneck barnacles and other outer coast prey are conjunction with data on size-specific predation risk, thereby absent, small sea stars are abundant and are often the most offering direct evidence of predation as a mechanism for (if not the only) easily removed and consumed intertidal these patterns. In addition, we describe parallel patterns in prey available to gulls. Although we observed gulls feeding the size and density of individuals among habitat types for upon other marine invertebrates during our observations at two co-occurring consumers with the potential to compete low tide, such as mussels and crabs, sea stars appeared to both intraspecifically and interspecifically for prey resour- be their primary prey. ces. Our results have implications for studies that examine Evasterias appeared to be more susceptible to predation predator–predator and predator–prey interactions within by gulls than Pisaster, as 88 % of sea stars consumed by these intertidal communities. gulls in boulder habitats were Evasterias, despite approx- imately equal densities of Pisaster and Evasterias in this Acknowledgments The authors thank D. Kimbro, R. Hughes, habitat type. This difference in susceptibility is likely due H. Feder, and three anonymous reviewers for constructive reviews; A. Titmus, A. Rudd, and M. Santos for survey data; and S. Reller, to the greater attachment strength of Pisaster relative to J. Elliott, G. Elliott, L. Elliott, M. Jones, T. McFarland, A. Boyd, and Evasterias, as well as the ability of gulls to consume larger C. Moore for assistance with field surveys. Surveys in the San Juan Evasterias than Pisaster in terms of arm length (up to Islands were conducted out of Friday Harbor Laboratories, and we 12 cm, as opposed to 9 cm). Weaker attachment of Evas- thank the director and staff for their excellent support. Funding was provided by a 2009 McCormick Undergraduate Summer Research terias would make this species easier for gulls to remove, Grant from the University of Puget Sound to TLR and a McCormick which is consistent with our field observations. Addition- grant from the University of Puget Sound to JKE. The authors declare ally, gulls were capable of pulling single arms off large that they have no conflict of interest. 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